The Oryza sativa Stress Associated Protein (OsSAP) Promoter Modulates Gene Expression in Response To Abiotic Stress by Utilizing Cis Regulatory Elements Within The Promoter Region
Keywords:
Abiotic stress, arabidopsis, β-glucuronidase (GUS), cis-regulatory elements, promoter, rice, Stress Associated Protein 4Abstract
The occurrence of extreme weather patterns induced by climate change has resulted in abiotic stress problems impacting the growth and productivity of plants. Rice (Oryza sativa), a staple food source for most Asians, is similarly affected by these challenges. Previous studies have identified the Oryza sativa Stress Associated Protein (OsSAP) genes to play a significant role in responding to abiotic stress. Among the 18 Stress Associated Protein members, OsSAP4 was highly expressed during drought and salinity conditions. Therefore, further experiments have been conducted, focusing specifically on the promoter region, to comprehend its regulation in response to abiotic stresses. Various types of cis-elements binding sites have been identified within the OsSAP4 promoter, encompassing MYB, CAMTA, CPP, C3H, HDZIP, bZIP, WRKY, and ERF. However, promoter analysis revealed that the distribution of the Cis-Regulatory elements bound by the Ethylene Response Factor (ERF) was the most prominent in the OsSAP4 promoter. Consequently, an analysis of promoter regulation was conducted using GUS reporter in Arabidopsis thaliana (A. thaliana) on two different sizes of OsSAP4 promoter sequences, each containing different quantities of ERF transcription factor binding sites. A noticeable difference in GUS staining activity was observed between pOsSAP4(1524 pb)::GUS and pOsSAP4(460 pb)::GUS, where pOsSAP4(1524 pb)::GUS exhibited higher GUS staining activity than pOsSAP4(460 pb)::GUS. The differences in GUS staining analysis are evident at the vegetative stage (leaf), silique, and inflorescence stages. This implies the participation of various other cis-element binding sites that influence the expression pattern of the OsSAP4 promoter during abiotic stress.
Downloads
Metrics
References
Agarwal, M., Hao, Y., Kapoor, A., Dong, C.H., Fujii, H., Zheng, X. & Zhu, J.K. 2006. A R2R3 type MYB transcription factor is involved in the cold regulation of CBF genes and in acquired freezing tolerance. Journal of Biological Chemistry, 281(49): 37636-37645. DOI: https://doi.org/10.1074/jbc.M605895200
Baumann, K., DePaolis, A., Costantino, P. & Gualberti, G. 1999. The DNA binding site of the Dof protein NtBBF1 is essential for tissue-specific and auxin-regulated expression of the rolB oncogene in plants. Plant Cell, 11: 323-334. DOI: https://doi.org/10.2307/3870863
Brooks, E.G., Elorriaga, E., Liu, Y., Duduit, J.R., Yuan, G., Tsai, C.-J., Tuskan, G.A., Ranney, T.G., Yang, X. & Liu, W. 2023. Plant promoters and terminators for high-precision bioengineering. BioDesign Research, 5: 1-21. DOI: https://doi.org/10.34133/bdr.0013
Cheng, X., Xiong, R., Yan, H., Gao, Y., Liu, H., Wu, M. & Xiang, Y. 2019. The trihelix family of transcription factors: Functional and evolutionary analysis in Moso bamboo (Phyllostachys edulis). BMC Plant Biology, 19(1): 154. DOI: https://doi.org/10.1186/s12870-019-1744-8
Cohen, S.P. & Jan, E.L. 2019. Abiotic and biotic stresses induce a core transcriptome response in rice. Scientific Reports, 9: 6273. DOI: https://doi.org/10.1038/s41598-019-42731-8
Cominelli, E., Galbiati, M., Vavasseur, A., Conti, L., Sala, T., Vuylsteke, M., Leonhardt, N., Dellaporta, S.L. & Tonelli, C. 2005. A guard-cell-specific MYB transcription factor regulates stomatal movements and plant drought tolerance. Current Biology, 15(13): 1196-1200. DOI: https://doi.org/10.1016/j.cub.2005.05.048
Dahro, B., Wang, F., Peng, T. & Liu, J.H. 2016. PtrA/NINV, an Alkaline/neutral invertase gene of Poncirus trifoliata, confers enhanced tolerance to multiple abiotic stresses by modulating ROS levels and maintaining photosynthetic efficiency. BMC Plant Biology, 16: 76. DOI: https://doi.org/10.1186/s12870-016-0761-0
Das, A., Pramanik, K., Sharma, R., Gantait, S. & Banerjee, J. 2019. In-silico study of biotic and abiotic stress-related transcription factor binding sites in the promoter regions of rice germin-like protein genes. PLoS ONE, 14: e0211887. DOI: https://doi.org/10.1371/journal.pone.0211887
Deng, Z., Yang, Z., Liu, X., Dai, X., Zhang, J. & Deng, K. 2023. Genome-wide identification and expression analysis of C3H zinc finger family in potato (Solanum tuberosum L.). International Journal of Molecular Sciences, 24(16): 12888. DOI: https://doi.org/10.3390/ijms241612888
Dixit, A., Tomar, P., Vaine, E., Abdullah, H., Hazen, S. & Dhankher, O.P. 2018. A stress-associated protein, AtSAP13, from Arabidopsis thaliana provides tolerance to multiple abiotic stresses. Plant, Cell & Environment, 41: 1171-1185. DOI: https://doi.org/10.1111/pce.13103
Dixit, A.R. & Dhankher, O.P. 2011. A novel stress-associated protein "AtSAP10" from Arabidopsis thaliana confers tolerance to nickel, manganese, zinc, and high temperature stress. PLoS ONE, 6: 20921. DOI: https://doi.org/10.1371/journal.pone.0020921
Dolgikh, V.A., Pukhovaya, E.M. & Zemlyanskaya, E.V. 2019. Shaping ethylene response: The role of EIN3/EIL1 transcription factors. Frontiers in Plant Science, 10: 1030. DOI: https://doi.org/10.3389/fpls.2019.01030
Dos Santos, T.B., Ribas, A.F., de Souza, S.G.H., Budzinski, I.G.F. & Domingues, D.S. 2022. Physiological responses to drought, salinity, and heat stress in plants: A Review. Stresses, 2: 113-135. DOI: https://doi.org/10.3390/stresses2010009
Elhiti, M. & Stasolla, C. 2009. Structure and function of homodomain-leucine zipper (HD-Zip) proteins. Plant Signaling and Behavior, 4(2): 86-88. DOI: https://doi.org/10.4161/psb.4.2.7692
El-kereamy, A., Bi, Y.M., Ranathunge, K., Beatty, P.H., Good, A.G. & Rothstein, S.J. 2012. The rice R2R3-MYB transcription factor OsMYB55 is involved in the tolerance to high temperature and modulates amino acid metabolism. PLoS ONE, 7(12): e52030. DOI: https://doi.org/10.1371/journal.pone.0052030
Fang, S., Li, C., Li, S., Tang, J., Shi, H., Yang, T., Liang, M. & Liu, D. 2022. Genome-wide analyses of tea plant stress-associated proteins (SAPs) reveal the role of CsSAP12 in increased drought tolerance in transgenic tomatoes. Horticulturae, 8: 363. DOI: https://doi.org/10.3390/horticulturae8050363
Gai, W.X., Ma, X., Qiao, Y.M., Shi, B.H., Haq, S., Li, Q.H., Wei, A.M., Liu, K.K. & Gong, Z.H. 2020. Characterization of the bZIP transcription factor family in pepper (Capsicum annuum L.): CabZIP25 positively modulates the salt tolerance. Frontiers in Plant Science, 11: 1-18. DOI: https://doi.org/10.3389/fpls.2020.00139
Gibbs, D.J., Lee, S.C., Isa, N.M., Gramuglia, S., Fukao, T., Bassel, G.W., Correia, C.S., Corbineau, F., Theodoulou, F.L., Bailey-Serres, J. & Holdsworth, M.J. 2011. Homeostatic response to hypoxia is regulated by the N-end rule pathway in plants. Nature, 479: 415-418. DOI: https://doi.org/10.1038/nature10534
Gong, R., Cao, H., Zhang, J., Xie, K., Wang, D. & Yu, S. 2018. Divergent functions of the GAGA-binding transcription factor family in rice. Plant Journal, 94(1): 32-47. DOI: https://doi.org/10.1111/tpj.13837
Guo, J., Bai, X., Dai, K., Yuan, X., Guo, P., Zhou, M., Shi, W. & Hao, C. 2021. Identification of GATA transcription factors in Brachypodium distachyon and Functional Characterization of BdGATA13 in drought tolerance and response to gibberellins. Frontiers in Plant Science, 12: 763665. DOI: https://doi.org/10.3389/fpls.2021.763665
Guo, M., Liu, J.H., Ma, X., Luo, D.X., Gong, Z.H. & Lu, M.H. 2016. The plant heat stress transcription factors (HSFS): Structure, regulation, and function in response to abiotic stresses. Frontiers in Plant Science, 7(10): 114. DOI: https://doi.org/10.3389/fpls.2016.00114
Han, G., Lu, C., Guo, J., Qiao, Z., Sui, N., Qiu, N. & Wang, B. 2020. C2H2 zinc finger proteins: master regulators of abiotic stress responses in plants. Frontiers in Plant Science, 11: 115. DOI: https://doi.org/10.3389/fpls.2020.00115
Heidari, P., Ahmad, I.M. & Najafi, Z.H. 2015. In silico analysis of cis-regulatory elements on co-expressed genes. Journal of Biological and Environmental Sciences, 9: 1-9.
Hernández-Verdeja, T. & Lundgren, M.R. 2024. GOLDEN2-LIKE transcription factors: A golden ticket to improve crops. Plants People Planet, 6(1): 79-93. DOI: https://doi.org/10.1002/ppp3.10412
Huang, J., Zhao, X., Bürger, M., Wang, Y. & Chory, J. 2021. Two interacting ethylene response factors regulate heat stress response. Plant cell, 33(2): 338-357. DOI: https://doi.org/10.1093/plcell/koaa026
Husain, T., Fatima, A., Suhel, M., Singh, S., Sharma, A., Prasad, S.M. & Singh, V.P. 2020. A brief appraisal of ethylene signaling under abiotic stress in plants. Plant Signaling and Behavior, 15(9): 1782051. DOI: https://doi.org/10.1080/15592324.2020.1782051
Jan, A., Maruyama, K., Todaka, D., Kidokoro, S., Abo, M., Yoshimura, E., Shinozaki, K., Nakashima, K. & Yamaguchi-Shinozaki, K. 2013. OsTZF1, a CCCH-tandem zinc finger protein, confers delayed senescence and stress tolerance in rice by regulating stress-related genes. Plant Physiology, 161(3): 1202-1216. DOI: https://doi.org/10.1104/pp.112.205385
Jiang, J., Ma, S., Ye, N., Jiang, M., Cao, J. & Zhang, J. 2017. WRKY transcription factors in plant responses to stresses. Journal of Integrative Plant Biology, 59(2): 86-101. DOI: https://doi.org/10.1111/jipb.12513
Jin, J., Duan, J., Shan, C., Mei, Z., Chen, H., Feng, H., Zhu, J. & Cai, W. 2020. Ethylene insensitive3-like2 (OsEIL2) confers stress sensitivity by regulating OsBURP16, the β subunit of polygalacturonase (PG1β-like) subfamily gene in rice. Plant Science, 292: 110353. DOI: https://doi.org/10.1016/j.plantsci.2019.110353
Jin, R., Klasfeld, S., Zhu, Y., Fernandez Garcia, M., Xiao, J., Han, S.K., Konkol, A. & Wagner, D. 2021. LEAFY is a pioneer transcription factor and licenses cell reprogramming to floral fate. Nature Communications, 12: 626. DOI: https://doi.org/10.1038/s41467-020-20883-w
Kang, M., Fokar, M., Abdelmageed, H. & Allen, R.D. 2011. Arabidopsis SAP5 functions as a positive regulator of stress responses and exhibits E3 ubiquitin ligase activity. Plant Molecular Biology, 75: 451-466. DOI: https://doi.org/10.1007/s11103-011-9748-2
Khairulbahri, M. 2021. Analyzing the impacts of climate change on rice supply in West Nusa Tenggara, Indonesia. Heliyon, 7(12): 08515. DOI: https://doi.org/10.1016/j.heliyon.2021.e08515
Khoso, M.A., Hussain, A., Ritonga, F.N., Ali, Q., Channa, M.M., Alshegaihi, R.M., Meng, Q., Ali, M., Zaman, W., Brohi, R.D., Liu, F. & Manghwar, H. 2022. WRKY transcription factors (TFs): Molecular switches to regulate drought, temperature, and salinity stresses in plants. Frontiers in Plant Science 13: 1039329. DOI: https://doi.org/10.3389/fpls.2022.1039329
Krämer U. 2015. Planting molecular functions in an ecological context with Arabidopsis thaliana. Elife, 4: e06100. DOI: https://doi.org/10.7554/eLife.06100
Lata, C. & Prasad, M. 2011. Role of DREBs in regulation of abiotic stress responses in plants. Journal of Experimental Botany, 62(14): 4731-4748. DOI: https://doi.org/10.1093/jxb/err210
Lenka, S. & Kailash, B. 2019. Abiotic stress responsive cis-regulatory elements (CREs) in rice (Oryza sativa L.) and other plants. OSF, 98: 1-10. DOI: https://doi.org/10.31219/osf.io/n98t5
Li, J., Zhang, M., Sun, J., Mao, X., Wang, J., Wang, J., Liu, H., Zheng, H., Zhen, Z., Zhao, H. & Zou, D. 2019a. Genome-wide characterization and identification of trihelix transcription factor and expression profiling in response to abiotic stresses in rice (Oryza sativa L.). International Journal of Molecular Sciences, 20(2): 251. DOI: https://doi.org/10.3390/ijms20020251
Li, Q., Shen, Y., Guo, L., Wang, H., Zhang, Y., Fan, C. & Zheng, Y. 2019b. The EIL transcription factor family in soybean: Genome-wide identification, expression profiling and genetic diversity analysis. FEBS Open Bio, 9(4): 629-642. DOI: https://doi.org/10.1002/2211-5463.12596
Li, X., Han, M., Zhang, H., Liu, F., Pan, Y., Zhu, J., Liao, Z., Chen, X. & Zhang, B. 2022. Structure and biological functions of zinc finger proteins and their roles in hepatocellular carcinoma. Biomarker Research, 10: 2. DOI: https://doi.org/10.1186/s40364-021-00345-1
Liu, C., Xu, X., Kan, J., Cheng, Z.M., Chang, Y., Lin, J. & Li, H. 2020a. Genome- wide analysis of the C3H zinc finger family reveals its functions in salt stress responses of Pyrus betulaefolia. PeerJ, 8(6): e9328. DOI: https://doi.org/10.7717/peerj.9328
Liu, J.X., Srivastava, R., Che, P. & Howell, S.H. 2007. Salt stress responses in Arabidopsis utilize a signal transduction pathway related to endoplasmic reticulum stress signaling. Plant Journal, 51(5): 897-909. DOI: https://doi.org/10.1111/j.1365-313X.2007.03195.x
Liu, S., Liv, Z., Liu, Y., Li, L. & Zhang, L. 2018. Network analysis of ABA-dependent and ABA-independent drought responsive genes in Arabidopsis thaliana. Genetics and Molecular Biology, 41(3): 624-637. DOI: https://doi.org/10.1590/1678-4685-gmb-2017-0229
Liu, Y., Jia, Z., Li, X., Wang, Z., Chen, F., Mi, G., Forde, B., Takahashi, H. & Yuan, L. 2020b. Involvement of a truncated MADS-box transcription factor zmtmm1 in root nitrate foraging. Journal of Experimental Botany, 71(15): 4547-4561. DOI: https://doi.org/10.1093/jxb/eraa116
Mangeon, A., Lin, W.C. & Springer, P.S. 2012. Functional divergence in the Arabidopsis LOB-domain gene family. Plant Signal Behavior, 7: 1544-1547. DOI: https://doi.org/10.4161/psb.22320
Meenakshi, K.A., Kumar, V., Dubey, A.K., Narayan, S., Sawant, S.V., Pande, V., Shirke, P.A. & Sanyal, I. 2022. CAMTA transcription factor enhances salinity and drought tolerance in chickpea (Cicer arietinum L.). Plant Cell, Tissue and Organ Culture, 148: 319-330. DOI: https://doi.org/10.1007/s11240-021-02191-3
Melo, B.P. Moura, S.M., Morgante, C.V., Pinheiro, D.H., Alves, N.S.F., Rodrigues-Silva, P.L., Lourenço-Tessutti, I.T., Andrade, R.V., Fragoso, R.R. & Grossi-de-Sa, M.F. 2021. Regulated promoters applied to plant engineering: an insight over promising soybean promoters under biotic stress and their cis-elements. Biotechnology Research and Innovation, 5(1): e2021005. DOI: https://doi.org/10.4322/biori.202105
Müller, M. & Munné-Bosch, S. 2015. Ethylene response factors: A key regulatory hub in hormone and stress signaling. Plant Physiology, 169: 32-41. DOI: https://doi.org/10.1104/pp.15.00677
Nan, H., Lin, Y., Wang, X. & Gao, L. 2021. Comprehensive genomic analysis and expression profiling of cysteine-rich polycomb-like transcription factor gene family in tea tree. Horticultural Plant Journal, 7(5): 469-478. DOI: https://doi.org/10.1016/j.hpj.2021.03.001
Nanjareddy, K., Arthikala, M.K., Aguirre, A.L., Gómez, B.M. & Lara, M. 2017. Plant promoter analysis: Identification and characterization of root nodule specific promoter in the common bean. Journal of Visualized Experiments, 130: 1-6. DOI: https://doi.org/10.3791/56140
Peleg, Z. & Eduardo, B. 2011. Hormone Balance and Abiotic Stress Tolerance in Crop Plants. Current Opinion in Plant Biology, 14: 95-290. DOI: https://doi.org/10.1016/j.pbi.2011.02.001
Qu, Y., Kong, W., Wang, Q. & Fu, X. 2021. Genome-wide identification mikc-type mads-box gene family and their roles during development of floral buds in wheel wingnut (Cyclocarya paliurus). International Journal of Molecular Sciences, 22(18): 10128. DOI: https://doi.org/10.3390/ijms221810128
Rahman, H., Yang, J., Xu, Y.P., Munyampundu, J.P. & Cai, X.Z. 2016. Phylogeny of plant CAMTAs and role of AtCAMTAs in nonhost resistance to Xanthomonas oryzae pv. oryzae. Frontiers in Plant Science 7: 177. DOI: https://doi.org/10.3389/fpls.2016.00177
Ramakrishna, A. & Ravishankar, G.A. 2011. Influence of abiotic stress signals on secondary metabolites in plants. Plant Signaling and Behavior, 6: 1720-1731. DOI: https://doi.org/10.4161/psb.6.11.17613
Reyes, J.C., Muro-Pastor, M.I. & Florencio, F.J. 2004. The GATA family of transcription factors in arabidopsis and rice. Plant Physiology, 134(4): 1718-1732. DOI: https://doi.org/10.1104/pp.103.037788
Roslan, N.F, Rashid, N.A., Suka, I.E., Taufik, N., Abdullah, N.S., Asruri, M.B., Toni, B., Sukiran, N.L., Zainal, Z. & Isa, N.M. 2017. Enhanced tolerance to salinity stress and ABA is regulated by Oryza sativa Stress Associated Protein 8 (OsSAP8). Australian Journal of Crop Science, 11: 853-860. aracterization and functional study of stress-associated protein in rice and Arabidopsis. Malaysian Applied Biology, 52(3): 73-86. DOI: https://doi.org/10.55230/mabjournal.v52i3.2705
Seo, Y.J., Park, J.B., Cho, Y.J., Jung, C., Seo, H.S., Park, S.K., Nahm, B.H. & Song, J.T. 2010. Overexpression of the ethylene-responsive factor gene BrERF4 from Brassica rapa increases tolerance to salt and drought in Arabidopsis plants. Molecules and Cells, 30(3): 271-277. DOI: https://doi.org/10.1007/s10059-010-0114-z
Shah, L., Sohail, A., Ahmad, R., Cheng, S., Cao, L. & Wu, W. 2022. The roles of MADS-Box Genes from root growth to maturity in Arabidopsis and rice. Agronomy, 12(3): 582. DOI: https://doi.org/10.3390/agronomy12030582
Shim, D., Hwang, J.U., Lee, J., Lee, S., Choi, Y., An, G., Martinoia, E. & Lee, Y. 2009. Orthologs of the class A4 heat shock transcription factor HsfA4a confer cadmium tolerance in wheat and rice. Plant Cell, 21(12): 4031-4043. DOI: https://doi.org/10.1105/tpc.109.066902
Sun, J., Jiang, H., Xu, Y., Li, H., Wu, X., Xie, Q. & Li, C. 2007. The CCCH-type zinc finger proteins AtSZF1 and AtSZF2 regulate salt stress responses in Arabidopsis. Plant and Cell Physiology, 48(8): 1148-1158. DOI: https://doi.org/10.1093/pcp/pcm088
Sun, J., Sun, Y., Ahmed, R.I., Ren, A. & Xie, M. 2019. Research progress on plant RING-finger proteins. Genes, 10: 973. DOI: https://doi.org/10.3390/genes10120973
Sun, Y., Jia, X., Chen, D., Fu, Q., Chen, J., Yang, W., Yang, H. & Xu, X. 2023. Genome wide identification and expression analysis of cysteine-rich polycomb-like protein (CPP) gene family in tomato. International Journal of Molecular Sciences, 24(6): 5762. DOI: https://doi.org/10.3390/ijms24065762
Theune, M.L., Bloss, U., Brand, L.H., Ladwig, F. & Wanke, D. 2019. Phylogenetic analyses and GAGA-motif binding studies of BBR/BPC proteins lend to clues in GAGA-MOTIF recognition and a regulatory role in brassinosteroid signaling. Frontiers in Plant Science, 10: 466. DOI: https://doi.org/10.3389/fpls.2019.00466
Ullah, A., Muhammad, A., Shamsu, A.Z., Qian, Z., Lujian, Z., Yu, Y. & Fangmin, C. 2019. Abiotic stresses intervene with ABA signaling to induce destructive metabolic pathways leading to death: Premature leaf senescence in plants. International Journal of Molecular Sciences, 10: 256. DOI: https://doi.org/10.3390/ijms20020256
Ullah, U., Buttar, Z.A., Shalmani, A., Muhammad, I., Ud-Din, A. & Ali, H. 2022. Genome-wide identification and expression analysis of CPP-like gene family in Triticum aestivum L. under different hormone and stress conditions. Open Life Sciences, 17(1): 544-562. DOI: https://doi.org/10.1515/biol-2022-0051
Urao, T., Yamaguchi-Shinozaki, K., Urao, S. & Shinozaki, K. 1993. An Arabidopsis myb homolog is induced by dehydration stress and its gene product binds to the conserved MYB recognition sequence. Plant Cell, 5(11): 1529-1539. DOI: https://doi.org/10.1105/tpc.5.11.1529
Villao-Uzho, L., Chávez-Navarrete, T., Pacheco-Coello, R., Sánchez-Timm, E. & Santos-Ordóñez, E. 2023. Plant promoters: Their identification, characterization, and role in gene regulation. Genes, 14(6):1226. DOI: https://doi.org/10.3390/genes14061226
Waltner, J.K., Peterson, F.C., Lytle, B.L. & Volkman, B.F. 2005. Structure of the B3 domain from Arabidopsis thaliana protein At1g16640. Protein Science, 14(9): 2478-2483. DOI: https://doi.org/10.1110/ps.051606305
Wang, T., Gao, X., Chen, S., Li, D., Chen, S., Xie, M., Xu, Z. & Yang, G. 2021. Genome-wide identification and expression analysis of ethylene responsive factor family transcription factors in Juglans regia. PeerJ, 9: 17. DOI: https://doi.org/10.7717/peerj.12429
Wang, X., Niu, Y. & Zheng, Y. 2021. Multiple functions of myb transcription factors in abiotic stress responses. International Journal of Molecular Sciences, 22(11): 6125. DOI: https://doi.org/10.3390/ijms22116125
Wang, X., Zou, B., Shao, Q., Cui, Y., Lu, S., Zhang, Y., Huang, Q., Huang, J. & Hua, J. 2018. Natural variation reveals that OsSAP16 controls low-temperature germination in rice. Journal of Experimental Botany, 69: 413-421. DOI: https://doi.org/10.1093/jxb/erx413
Waqas, M.A., Kaya, C., Riaz, A., Farooq, M., Nawaz, I., Wilkes, A. & Li, Y. 2019. Potential mechanisms of abiotic stress tolerance in crop plants induced by Thiourea. Frontiers in Plant Science, 10: 1336. DOI: https://doi.org/10.3389/fpls.2019.01336
Wei, M., Li, H., Wang, Q., Liu, R., Yang, L. & Li, Q. 2023. Genome-wide identification and expression profiling of B3 transcription factor genes in Populus alba X Populus glandulosa. Frontiers in Plant Science, 14: 1-15. DOI: https://doi.org/10.3389/fpls.2023.1193065
Wu, X., Tao, M., Meng, Y., Zhu, X., Qian, L., Shah, A., Wang, W. & Cao, S. 2019. The role of WRKY47 gene in regulating selenium tolerance in Arabidopsis thaliana. Plant Biotechnology Reports, 14(1): 121-129. DOI: https://doi.org/10.1007/s11816-019-00560-1
Xiao, P., Feng, J.W., Zhu, X.T. & Gao, J. 2021. Evolution analyses of CAMTA transcription factor in plants and its enhancing effect on cold-tolerance. Frontiers in Plant Science, 12: 1-15. DOI: https://doi.org/10.3389/fpls.2021.758187
Xie, Z., Nolan, T.M., Jiang, H. & Yin, Y. 2019. AP2/ERF transcription factor regulatory networks in hormone and abiotic stress responses in Arabidopsis. Frontiers in Plant Science, 10: 228. DOI: https://doi.org/10.3389/fpls.2019.00228
Xiong, H., Li, J., Liu, P., Duan, J., Zhao, Y., Guo, X., Li, Y., Zhang, H., Ali, J. & Li, Z. 2014. Overexpression of OsMYB48-1, a novel MYB-related transcription factor, enhances drought and salinity tolerance in rice. PLoS ONE, 9(3): e92913. DOI: https://doi.org/10.1371/journal.pone.0092913
Xu, Z.S., Chen, M., Li, L.C. & Ma, Y.Z. 2011. Functions and application of the AP2/ERF transcription factor family in crop improvement. Journal of Integrative Plant Biology, 53(7): 570-585. DOI: https://doi.org/10.1111/j.1744-7909.2011.01062.x
Yamaguchi, N. 2021. LEAFY, a pioneer transcription factor in plants: A mini-review. Frontiers in Plant Science, 12: 701406. DOI: https://doi.org/10.3389/fpls.2021.701406
Yang, K., Li, C.Y., An, J.P., Wang, D.R., Wang, X., Wang, C.K. & You, C.X. 2021a. The C2H2-type zinc finger transcription factor MdZAT10 negatively regulates drought tolerance in apple. Plant Physiology and Biochemistry, 167: 390- 399. DOI: https://doi.org/10.1016/j.plaphy.2021.08.014
Yang, T., Guo, L., Ji, C., Wang, H., Wang, J., Zheng, X., Xiao, Q. & Wu, Y. 2021b. The B3 domain-containing transcription factor ZmABI19 coordinates expression of key factors required for maize seed development and grain filling. Plant Cell, 33(1): 104-128. DOI: https://doi.org/10.1093/plcell/koaa008
Yong, Y., Zhang, Y. & Lyu, Y. 2019. A myb-related transcription factor from Lilium lancifolium L. (LLMYB3) is involved in anthocyanin biosynthesis pathway and enhances multiple abiotic stress tolerance in Arabidopsis thaliana. International Journal of Molecular Sciences, 20(13): 3195. DOI: https://doi.org/10.3390/ijms20133195
Yoshida, T., Sakuma, Y., Todaka, D., Maruyama, K., Qin, F., Mizoi, J., Kidokoro, S., Fujita, Y., Shinozaki, K. & Yamaguchi-Shinozaki, K. 2008. Functional analysis of an Arabidopsis heat-shock transcription factor HsfA3 in the transcriptional cascade downstream of the DREB2A stress-regulatory system. Biochemical and Biophysical Research Communications, 368(3): 515-521. DOI: https://doi.org/10.1016/j.bbrc.2008.01.134
Yu, L., Chen, X., Wang, Z., Wang, S., Wang, Y., Zhu, Q., Li, S. & Xiang, C. 2013. Arabidopsis enhanced drought tolerance1/HOMEODOMAIN GLABROUS11 confers drought tolerance in transgenic rice without yield penalty. Plant Physiology, 162(3): 1378-1391. DOI: https://doi.org/10.1104/pp.113.217596
Yuan, X., Huang, P., Wang, R., Li, H., Liv, X., Duan, M., Tang, H., Zhang, H. & Huang, J. 2018. A zinc finger transcriptional repressor confers pleiotropic effects on rice growth and drought tolerance by down-regulating stress-responsive genes. Plant and Cell Physiology, 59(10): 2129-2142. DOI: https://doi.org/10.1093/pcp/pcy133
Zhang, H., Xie, P., Xu, X., Xie, Q. & Yu, F. 2021. Heterotrimeric G protein signalling in plant biotic and abiotic stress response. Plant Biology, 23: 20-30. DOI: https://doi.org/10.1111/plb.13241
Zhang, Z., Chen, X., Guan, X., Liu, Y., Chen, H., Wang, T., Mouekouba, L.D.O., Li, J. & Wang, A. 2014. A genome-wide survey of homeodomain-leucine zipper genes and analysis of cold-responsive HD-Zip I members' expression in tomato. Bioscience, Biotechnology and Biochemistry, 78(8): 1337-1349. DOI: https://doi.org/10.1080/09168451.2014.923292
Zhao, S., Zhang, Q., Liu, M., Zhou, H., Ma, C. & Wang, P. 2021. Regulation of plant responses to salt stress. International Journal of Molecular Sciences, 22(9): 4609. DOI: https://doi.org/10.3390/ijms22094609
Zhou, E., Zhang, Y., Wang, H., Jia, Z., Wang, X., Wen, J., Shen, J., Fu, T. & Yi, B. 2022. Identification and characterization of the MIKC-Type MADS-Box gene family in Brassica napus and its role in floral transition. International Journal of Molecular Sciences, 23(8): 4289. DOI: https://doi.org/10.3390/ijms23084289
Published
How to Cite
Issue
Section
Any reproduction of figures, tables and illustrations must obtain written permission from the Chief Editor (wicki@ukm.edu.my). No part of the journal may be reproduced without the editor’s permission
Funding data
-
Ministry of Higher Education, Malaysia
Grant numbers FRGS/1/2020/STG01/UKM/02/6 -
Universiti Kebangsaan Malaysia
Grant numbers GUP-2018-115